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Gonadotrophin-releasing hormone agonist raises plasma concentrations of progestogens and enhances milt fluidity in male Atlantic halibut (Hippoglossus hippoglossus)

Abstract

In two separate spawning seasons, spermiating male Atlantic halibut were implanted with pellets containing gonadotrophin-releasing hormone agonist (GnRHa). Males were bled repeatedly, and milt samples were collected. Blood samples were assayed for free and conjugated steroids: testosterone, 11-ketotestosterone, 17,20α-dihydroxy-4-pregnen-3-one (17,20α-P), 17,20β-dihydroxy-4-pregnen-3-one (17,20β-P), 17,20β,21-trihydroxy-4-pregnen-3-one and steroids with a 17,20β configuration. Towards the end of the first season, pellets were implanted into three wild-caught and three hatchery-reared males. No control fish were available. The major progestogen in plasma was identified as sulphated 5β-pregnane-3β,17,20β-triol (3β,17,20β-P-5β-S). Concentrations of this steroid were stimulated by the GnRHa. Sulphated 17,20β-P was also identified in the plasma, but at 10-fold lower concentrations than 3β,17,20β-P-5β-S. In the middle of the second season, pellets were implanted into five hatchery-reared males; five unimplanted males were used as controls. Levels of androgens fell following GnRHa treatment, levels of progestogens rose briefly, and there was a significant increase in the fluidity of the milt. Of all the measured steroids, free and sulphated 17,20α-P showed the best correlation with milt fluidity.

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References

  • Alveriño, J.M.R. and Peleteiro, J.B. 1993. Inducción y sincronización de la puesta en el rodaballo (Scophthalmus maximus) con LHRHa: influencia del estado de desarrollo gonadal. In: Proc. IVth National Congress on Aquaculture. Illa de Arousa (Vilanova de Arousa), Spain. pp. 31-36. Edited by A. Cerviño, A. Landín, A. de Coo, A. Guerra and M. Torre. Centro de Investigacións Marinas, Vilagarcía de Arousa (Pontevedra).

    Google Scholar 

  • Asahina, K., Barry, T.P., Aida, K., Fusetani, N. and Hanyu, I. 1990. Biosynthesis of 17?,20?-dihydroxy-4-pregnen-3-one from 17?-hydroxyprogesterone by spermatozoa of the common carp, Cyprinus carpio. J. Exp. Zool. 255: 244-249.

    Google Scholar 

  • Avila, E.M. 1984. Hormone-induced spawning and embryonic development of the rabbitfish, Siganus vermiculatus (Pisces: Siganidae). Philipp. Sci. 21: 75-108.

    Google Scholar 

  • Berlinsky, D.L., King V.W., Hodson, R.G. and Sullivan, C.V. 1997.Hormone induced spawning of summer flounder Paralichthys dentatus. J. World Aquacult. Soc. 28: 79-86.

    Google Scholar 

  • Berlinsky, D.L., King V. W., Smith, T.I.J., Hamilton II, R.D., Holloway, J.J. and Sullivan, C.V. 1996. Induced ovulation of southern flounder Paralichthys lethostigma using gonadotropin releasing hormone analogue implants. J. World Aquacult. Soc. 27: 143-152.

    Google Scholar 

  • Billard, R., Fostier, A., Weil, C. and Breton, B. 1982. Endocrine control of spermatogenesis in teleost fish. Can. J. Fish. Aquat. Sci. 39: 65-79.

    Google Scholar 

  • Borg, B. 1994. Androgens in teleost fishes. Comp. Biochem. Physiol. 109C: 219-245.

    Google Scholar 

  • Canario, A.V.M. and Scott, A.P. 1989. Synthesis of 20?-hydroxylated steroids by ovaries of the dab (Limanda limanda. Gen. Comp. Endocrinol. 76: 147-158.

    Google Scholar 

  • Clearwater, S.J. and Crim, L.W. 1995. Milt quality and quantity produced by yellowtail flounder (Pleuronectes ferrugineus) following GnRH-analogue treatment by microspheres or pellet. In: Proc. Vth Symp. on the Reproductive Physiology of Fish. Austin. p. 113. Edited by F.W. Goetz and P. Thomas. Fish Symposium 95, Austin.

  • Clemens, H.P. and Grant, F.B. 1965. The seminal thinning response of carp (Cyprinus carpio) and rainbow trout (Salmo gairdnerii) after injections of pituitary extracts. Copeia 2: 174-177.

    Google Scholar 

  • Di Matteo, L., Minucci, S., Fasano, S., D'Antonio, M., Pierantoni, R. and Chieffi, G. 1990. Indirect evidence for a physiological role exerted by a ‘testicular gonadotropin-releasing hormone’ in the frog, Rana esculenta. Gen. Comp. Endocrinol. 79: 147-153.

    Google Scholar 

  • El-Etr, M., Akwa, Y., Robel, P., Baulieu, E.E. 1998. Opposing effects of different steroid sulfates on GABAA receptor-mediated chlorine uptake. Brain Res. 790: 334-338.

    Google Scholar 

  • Fostier, A., Jalabert, B., Billard, R., Breton, B. and Zohar, Y. 1983. The gonadal steroids. In: Fish Physiology. Vol. IX, Part A. pp. 277-372. Edited by W.S. Hoar, D.J. Randall and E.M. Donaldson. Academic Press, New York.

    Google Scholar 

  • Garcia, L.M.B. 1993. Sustained production of milt in rabbitfish, Siganus guttatus Bloch, by weekly injection of luteinizing hormone-releasing hormone analogue (LHRHa). Aquaculture 113: 261-167.

    Google Scholar 

  • Garcia-Abiado, M.A.R., Merculio, J.G. and Mair, G.C. 1996. The effect of luteinizing hormone-releasing hormone analogue (LHRHa) on sperm count of Oreochromis niloticus (L.). Aquacult. Res. 27: 95-100.

    Google Scholar 

  • Harmin, S.A. and Crim, L.W. 1992. Gonadotropic hormonereleasing hormone analog (GnRH-A) induced ovulation and spawning in female winter flounder, Pseudopleuronectes americanus (Walbaum). Aquaculture 104: 375-390.

    Google Scholar 

  • Harmin, S.A. and Crim, L.W. 1993. Influence of gonadotropic hormone-releasing hormone analog (GnRH-A) on plasma sex steroid profiles and milt production in male winter flounder, Pseudopleuronectes americanus (Walbaum). Fish Physiol. Biochem. 10: 399-407.

    Google Scholar 

  • Harmin, S.A., Crim, L.W. and Evans, D.M. 1987. The influence of [D-Ala6, Pro9-NHEt]LHRH (LHRHa) treatment on plasma sex steroid profiles of winter flounder, Pseudopleuronectes americanus during gonadal recrudescence. In: Proc. IIIrd Int. Symp. on Reproductive Physiology of Fish. St. John's p. 200. Edited by D.R. Idler, L.W. Crim and J.M. Walsh. Memorial University Press, St. John's.

    Google Scholar 

  • Hawkinson, K.E., Kimborough, C.L., McCauley, L.D., Bolger, M.B., Lan, N.C., Gee, K.W. 1994. The neuroactive steroid 3?-hydroxy-5?-pregnan-20-one is a two-component modulator of ligand binding the GABAA receptor. Eur. J. Pharmacol. Mol. Pharmacol. Sect. 269: 157-163.

    Google Scholar 

  • Hirano, Y., Miyazaki, H., Higashidate, S. and Nakayama, F. 1987. Analysis of 3-sulfated and nonsulfated bile acids by one-step solvolysis and high performance liquid chromatography. J. Lipid Res. 28: 1524-1529.

    Google Scholar 

  • Inbaraj, R.M., Scott, A.P. and Vermeirssen, E.L.M. 1997. Use of a radioimmunoassay which detects C21 steroids with a 5?-reduced, 3?-hydroxylated configuration to identify and measure steroids involved in final oocyte maturation in female plaice (Pleuronectes platessa. Gen. Comp. Endocrinol. 105: 50-61.

    Google Scholar 

  • Kime, D.E. 1993. ‘Classical’ and ‘non-classical’ reproductive steroids in fish. Rev. Fish Biol. Fish. 3: 160-180.

    Google Scholar 

  • King V, W., Thomas, P., Harrell, R.M., Hodson, R.G. and Sullivan, C.V. 1994. Plasma levels of gonadal steroids during final oocyte maturation of striped bass, Morone saxatilis L. Gen. Comp. Endocrinol. 95: 178-191.

    Google Scholar 

  • Larsson, D.G.J., Mylonas, C.C., Zohar, Y. and Crim, L.W. 1997. Gonadotropin-releasing hormone analogue (GnRH-A) induces multiple ovulations of high-quality eggs in a cold-water, batch-spawning teleost, the yellowtail flounder (Pleuronectes ferrugineus). Can. J. Fish. Aquat. Sci. 54: 1957-1964.

    Google Scholar 

  • Lee, S.T.L., Kime, D.E., Lam, T.J. and Tan, C.H. 1998. Synthesis of 17,20? /?-dihydroxy-4-pregnen-3-one and 5?-pregnanes in spermatozoa of primary and 17?-methyltestosterone-induced secondary male grouper (Epinephelus coioides). Gen. Comp. Endocrinol. 112: 1-9.

    Google Scholar 

  • Mangor-Jensen, A., Harboe, T., Shields, R.J., Gara, B. and Naas, K.E. 1998. Review of halibut larvae cultivation literature, including a bibliography. Aquacult. Res. 29: 857-886.

    Google Scholar 

  • Methven, D.A. and Crim, L.W. 1991. Seasonal changes in spermatocrit, plasma sex steroids, and motility of sperm from Atlantic halibut (Hippoglossus hippoglossus). In: Proc. IVth Int. Symp. on the Reproductive Physiology of Fish. Norwich. p. 170. Edited by A.P. Scott, J.P. Sumpter, D.E. Kime and M.S. Rolfe. FishSymp 91, Sheffield.

  • Methven, D.A., Crim, L.W., Norberg, B., Brown, J.A., Goff, G.P. and Huse, I. 1992. Seasonal reproduction and plasma levels of sex steroids and vitellogenin in Atlantic halibut (Hippoglossus hippoglossus). Can. J. Fish. Aquat. Sci. 49: 754-759.

    Google Scholar 

  • Miura, T., Yamauchi, K., Takahashi, H. and Nagahama, Y. 1992. The role of hormones in the acquisition of sperm motility in salmonid fish. J. Exp. Zool. 261: 359-363.

    Google Scholar 

  • Mylonas, C.C., Scott, A.P., Vermeirssen, E.L.M. and Zohar, Y. 1997. Changes in plasma gonadotropin II and sex steroid hormones, and sperm production of striped bass after treatment with controlled-release gonadotropin-releasing hormone agonist-delivery systems. Biol. Reprod. 57: 669-675.

    Google Scholar 

  • Nagahama, Y. 1994. Endocrine regulation of gametogenesis in fish. Int. J. Dev. Biol. 38: 217-229.

    Google Scholar 

  • Norberg, B., Valkner, V., Huse, J., Karlsen, I. and Grung, G.L. 1991. Ovulatory rhythms and egg viability in the Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 97: 365-371.

    Google Scholar 

  • Pankhurst, N.W. 1994. Effects of gonadotropin releasing hormone analogue, human chorionic gonadotropin and gonadal steroids on milt volume in the New Zealand snapper, Pagrus auratus (Sparidae). Aquaculture 125: 185-197.

    Google Scholar 

  • Pati, D. and Habibi, H.R. 1993. Gonadotropin-releasing hormone (GnRH) binding characteristics in the testis of goldfish (Carassius auratus). J. Exp. Zool. 267: 155-163.

    Google Scholar 

  • Peter, R.E., Chang, J.P., Nahorniak, C.S., Omeljaniuk, R.J., Shih, S.H., Sokolowska, M. and Billard, R. 1986. Interaction of catecholamines and GnRH in regulation of gonadotropin secretion in teleost fish. Recent Prog. Horm. Res. 42: 513-545.

    Google Scholar 

  • Saad, A. and Billard, R. 1987. Spermatozoa production and volume of semen collected after hormonal stimulation in the carp, Cyprinus carpio. Aquaculture 65: 67-77.

    Google Scholar 

  • SAS Institute Inc. 1990. ‘sAS/STAT User's Guide’ Release 6.03, p.1028. SAS Institue Inc., Cary, NC.

    Google Scholar 

  • Scott, A.P. and Canario, A.V.M. 1987. Status of oocyte maturationinducing steroids in teleosts. In: Proc. IIIrd Int. Symp. on Reproductive Physiology of Fish. St. John's. pp. 224-234. Edited by D.R. Idler, L.W. Crim and J.M. Walsh. Memorial University Press, St. John's.

    Google Scholar 

  • Scott, A.P., Inbaraj, R.M. and Vermeirssen, E.L.M. 1997. Use of a radioimmunoassay which detects C21 steroids with a 17,20?-dihydroxyl configuration to identify and measure steroids involved in final oocyte maturation in female plaice (Pleuronectes platessa). Gen. Comp. Endocrinol. 105: 62-70.

    Google Scholar 

  • Scott, A.P., Mackenzie, D.S. and Stacey, N.E. 1984. Endocrine changes during natural spawning in the white sucker, Catostomus commersoni. II. Steroid hormones. Gen. Comp. Endocrinol. 56: 349-359.

    Google Scholar 

  • Scott, A.P., Sheldrick, E.L. and Flint, A.P.F. 1982. Measurement of 17?,20?-dihydroxy-4-pregnen-3-one in plasma of trout (Salmo gairdneri Richardson): seasonal changes and response to salmon pituitary extract. Gen. Comp. Endocrinol. 46: 444-451.

    Google Scholar 

  • Scott, A.P., Sherwood, N.M., Canario, A.V.M. and Warby, C.M. 1991. Identification of free and conjugated steroids, including cortisol and 17?,20?-dihydroxy-4-pregnen-3-one, in the milt of Pacific herring, Clupea harengus pallasi. Can. J. Zool. 69: 104-110.

    Google Scholar 

  • Scott, A.P. and Sorensen, P.W. 1994. Time course of release of pheromonally active gonadal steroids and their conjugates by ovulatory goldfish. Gen. Comp. Endocrinol. 96: 309-323.

    Google Scholar 

  • Scott, A.P. and Vermeirssen, E.L.M. 1995. Research on reproductive priming pheromones in fish. In: Workshop Fish Pheromones: Origins and Modes of Action. Faro. pp. 15-23. Compiled by A.V.M. Canário and D.M. Power. University of Algarve, Faro, Portugal.

    Google Scholar 

  • Sharpe, R.M. 1982. Cellular aspects of the inhibitory actions of LHRH on the ovary and testis. J. Reprod. Fert. 64: 517-527.

    Google Scholar 

  • Sherwood, N.M., Crim, L.W., Carolsfeld, J. and Walters, S.M. 1988. Sustained hormone release. I. Characteristics of in vitro release of gonadotrophin-releasing hormone analogue (GnRH-A) from pellets. Aquaculture 74: 75-86.

    Google Scholar 

  • Shields, R.J., Gara, B. and Gillespie, M.J.S.G. 1999. A UK perspective on intensive hatchery production methods for Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 176: 15-25.

    Google Scholar 

  • Sorbera, L.A., Mylonas, C.C., Zanuy, S., Carrillo, M. and Zohar, Y. 1996. Sustained administration of GnRHa increases milt volume without altering sperm counts in the sea bass. J. Exp. Zool. 276: 361-368.

    Google Scholar 

  • Stacey, N., Cardwell, J. and Murphy, C. 1995. Hormonal pheromones in freshwater fishes: preliminary results of an electro-olfactogram survey. In Workshop Fish Pheromones: Origins and Modes of Action, University of Algarve. Faro. pp. 47-55. Compiled by A.V.M. Canário and D.M. Power. University of Algarve, Faro, Portugal.

    Google Scholar 

  • Stacey, N.E., Cardwell, J.R., Liley, N.R., Scot, A.P. and Sorensen, P.W. 1994. Hormones as sex pheromones in fish. In: Perspectives in Comparative Endocrinology. pp. 438-448. Edited by K.G. Davey, R.E. Peter and S.S. Tobe. National Research Council of Canada, Ottawa.

    Google Scholar 

  • Trant, J.M. and Thomas, P. 1989. Isolation of a novel maturationinducing steroid produced in vitro by ovaries of Atlantic croaker. Gen. Comp. Endocrinol. 75: 397-404.

    Google Scholar 

  • Vermeirssen, E.L.M., Scott, A.P., Mylonas, C.C. and Zohar, Y. 1998. Gonadotrophin-releasing hormone agonist stimulates milt fluidity and plasma concentrations of 17,20?-dihydroxylated and 5?-reduced, 3?-hydroxylated C21 steroids in male plaice (Pleuronectes platessa). Gen. Comp. Endocrinol. 112: 163-177.

    Google Scholar 

  • Weil, C. and Crim, L.W. 1983. Administration of LHRH analogues in various ways: effect on the advancement of spermiation in prespawning landlocked salmon, Salmo salar. Aquaculture 35: 103-115.

    Google Scholar 

  • Wiegand, M.D., Crim, L.W., Wilson, C.E., Hewitt, C.M. and Loewen, J.M. 1987. A study of oocyte development and induction of spawning in the winter flounder following LHRH analog implantation. In Proc. IIIrd Int. Symp. on Reproductive Physiology of Fish. St. John's. pp. 104-105. Edited by D.R. Idler, L.W. Crim and J.M. Walsh. Memorial University Press, St. John's.

    Google Scholar 

  • Yueh, W.-S., Lin, S.-F. and Chang, C.-F. 1990. Effects of LHRH-A and HCG on spermiation volume, concentration of milt and sex steroids in black porgy, Acanthopagrus schlegeli. J. Fish. Soc. Taiwan 17: 65-72.

    Google Scholar 

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Vermeirssen, E., Shields, R., Mazorra de Quero, C. et al. Gonadotrophin-releasing hormone agonist raises plasma concentrations of progestogens and enhances milt fluidity in male Atlantic halibut (Hippoglossus hippoglossus). Fish Physiology and Biochemistry 22, 77–87 (2000). https://doi.org/10.1023/A:1007820913009

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  • DOI: https://doi.org/10.1023/A:1007820913009

  • androgens
  • GnRHa
  • halibut
  • milt fluidity
  • progestogens
  • sperm
  • steroid conjugates